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Sediment Properties and Bacterial Community in Burrows of the Ghost Shrimp Pestarella Tyrrhena (Decapoda: Thalassinidea)

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Sediment Properties and Bacterial Community in Burrows of the Ghost Shrimp Pestarella Tyrrhena (Decapoda: Thalassinidea) AQUATIC MICROBIAL ECOLOGY Vol. 38: 181–190, 2005 Published February 9 Aquat Microb Ecol Sediment properties and bacterial community in burrows of the ghost shrimp Pestarella tyrrhena (Decapoda: Thalassinidea) Sokratis Papaspyrou1,*, Trine Gregersen2, Raymond P. Cox2, Maria Thessalou-Legaki1, Erik Kristensen3 1Department of Zoology–Marine Biology, Faculty of Biology, University of Athens, Panepistimiopolis, 157 84 Athens, Greece 2Department of Biochemistry and Molecular Biology, and 3Institute of Biology, University of Southern Denmark, 5230 Odense M, Denmark ABSTRACT: Chemical properties of burrow wall sediment from burrows of the thalassinidean shrimp Pestarella (=Callianassa) tyrrhena located at Vravrona Bay (Aegean Sea, Greece) were studied and found to be very different from the sediment surface and ambient anoxic sediment. P. tyrrhena burrow walls had significantly higher amounts of silt and clay, while total organic carbon (TOC) was up to 6 times higher than in surrounding sediment. Chlorophyll a (chl a) accounted for a small frac- tion of TOC and showed similar values in burrow walls and surface sediment, whereas the low chl a: chl a + phaeopigment ratio indicated the presence of more fresh material in the latter. Biopolymers (carbohydrates, proteins and lipids) were 4 to 11 times higher in burrow walls than in the surround- ing sediment, accounting for 47% of TOC. The low protein:carbohydrate ratio indicated that the high TOC in the burrow walls was caused by the presence of aged detritus of low nutritional quality, such as seagrass detritus. The distinct conditions along the burrow wall also affected the bacterial community and resulted in a 10-fold increase of bacterial abundance. Molecular fingerprints of the bacterial communities showed that the bacterial composition of the burrow wall was more similar to the ambient anoxic sediment and showed less seasonal change than the sediment surface. These results suggest that burrow walls have distinct properties and should not be considered merely as a simple extension of the sediment surface. KEY WORDS: Bioturbation · Organic matter · Seagrass detritus · Bacteria · PCR-DGGE · Pestarella tyrrhena Resale or republication not permitted without written consent of the publisher INTRODUCTION plex structures (Griffis & Suchanek 1991, Ziebis et al. 1996, Dworschak 2001). Biogenic structures, such as tubes and burrows, are a The burrow environment is usually very distinct and ubiquitous feature of aquatic environments. Tubes and differs from other parts of the sediment (surface and burrows are semi-permanent or permanent structures ambient anoxic sediment). Burrow walls are often rich in that differ in size, appearance and composition accord- organic matter of variable reactivity depending on its ing to the feeding habits, mode of life, mobility, as well origin, chemical composition, structure and age (Aller & as the size of infaunal species (Meadows 1991). Bur- Aller 1986, Reichardt 1988, de Vaugelas & Buscail 1990). rows range in length from a few mm (meiofauna) to The low diffusivity of burrow linings, when present, several meters (large polychaetes and crustaceans). reduces transport of solutes between the sediment and They may have vertical or horizontal orientation, be the burrow lumen, while the usually intermittent pattern branched or straight, and have either simple or com- of animal irrigation promotes very variable oxygen con- *Email: [email protected] © Inter-Research 2005 · www.int-res.com 182 Aquat Microb Ecol 38: 181–190, 2005 ditions in the burrows (Kristensen 1988, Ziebis et al. 24° 01’ E). The coast is lined by salt marshes and a sea- 1996, Furukawa 2001). The availability of labile organic sonal stream discharges near the head of the bay. The matter combined with steep chemical gradients and tidal amplitude in the area ranges from 10 to 30 cm and narrow redox zonation has a significant impact on the the largest part of the flat is exposed to the air during chemical and biological composition of the burrow spring low tides. The sediment in the sandflat consists environment. Bacterial abundances have been shown to mainly of moderately sorted medium to fine sand with be higher along burrow walls compared to either surface a median particle size of 0.2 mm and organic matter or ambient sediment (Aller & Aller 1986, Branch & content of 2.2%. The macrophyte vegetation is charac- Pringle 1987, Dworschak 2001). In addition, burrow walls terised by scattered occurrence of the seagrass show increased heterotrophic activity by both aerobic Cymodocea nodosa. Dead leaves of another seagrass, and anaerobic bacteria, resulting in increased rates Posidonia oceanica, are continuously transported into of organic matter decomposition (Aller & Aller 1986, the area from deeper waters. Mean salinity in the area Reichardt 1988, Gribsholt et al. 2003). ranges from 20 to 39‰ during the year and water Thalassinidean ghost shrimps have been recognised temperature from 11 to 29°C. in recent years as one of the most effective bioturbating Pestarella tyrrhena is the most abundant large bio- groups of macrofaunal organisms, with significant im- turbator in the intertidal and shallow subtidal area and pacts on the benthic environment (Griffis & Suchanek shows a mean yearly population density of 63 ± 9 ind. 1991, Reise 2002). Pestarella tyrrhena is an important m–2, and a maximum of 144 ind. m–2 (Thessalou-Legaki bioturbator, commonly found in muddy and fine sandy 1987). It occurs in the middle part of the sandflat, intertidal and shallow subtidal coastal sediments, avoiding both the wave-exposed seaward front and where it often creates dense monospecific populations. the muddier inshore salt marsh fringe that is charac- It is a selective deposit feeder that constructs deep and terised by large salinity variations (Thessalou-Legaki complex burrows, constantly digging new branches or 1987). The diversity and abundance of other benthic filling up existing ones (Dworschak 1987). P. tyrrhena macrofauna are generally low (A. Nicolaidou & increases the organic matter content in the sediment M. Thessalou-Legaki unpubl. data). and benthic metabolism by incorporating organic de- Sediment sampling. Sediment samples were col- tritus, such as seagrass debris, in burrow chambers lected at low tide in November 2001, and January, April (Dworschak 1987, 2001, Papaspyrou et al. 2004). In ad- and August 2002. Samples were collected from 3 differ- dition, it has been proposed that P. tyrrhena consoli- ent compartments associated with Pestarella tyrrhena dates the burrow walls with mucus (Dworschak 1983, burrows using a stainless steel spatula: burrow walls, 1998). However, detailed studies have not been made anoxic subsurface sediment adjacent to the burrows on the effect of P. tyrrhena on the distribution and com- (referred to as ‘ambient’) and the sediment surface. position of organic matter associated with the burrow, Undisturbed surface sediment was retrieved to a depth or its effects on the sediment microbial community. of 1 to 2 mm. Burrow wall and ambient sediment were The aims of this study were to investigate the abiotic sampled from 5 to 20 cm below the surface after expos- and biotic burrow environment of Pestarella tyrrhena ing burrows by digging. The burrow wall, defined as and to determine how sediment properties along the layer with a clearly visible difference in colour and burrow walls differ from the surroundings. For this texture from adjacent sediment, corresponding to a purpose, we collected seasonal samples from burrow radial distance of 1 to 2 mm, was recovered first. Sub- walls, surface sediment and anoxic sediment, to deter- sequently, the surrounding ambient sediment was mine particle size distribution, total organic carbon collected at the same depth, but away from the burrow. (TOC) content and relative contributions of major Sediment material was collected from at least 5 differ- organic compounds (proteins, carbohydrates and ent burrows, pooled together and analysed in triplicate, lipids), and phytopigments. In addition we studied the with the exception of bacterial abundance and parti- bacterial communities in burrow walls and the sur- culate iron pool analyses which were performed on rounding sediment by measuring bacterial abundance samples from individual burrows (see later). and obtaining molecular fingerprints of the bacterial Samples for determination of the sediment physico- community based on 16S rRNA gene sequences. chemical characteristics were stored in acid-washed Eppendorf tubes (10% HCl overnight, rinsed with Milli-Q water) and kept on ice until return to the labo- MATERIALS AND METHODS ratory, where they were immediately frozen at –80°C and subsequently freeze-dried. Samples for bacterial Study site. Sample collection was conducted in a DNA extraction were collected in sterile Eppendorf small (0.26 km2) intertidal-shallow subtidal sandflat tubes using a sterile stainless-steel spatula, kept on ice at Vravrona Bay, Aegean Sea, Greece (37° 56’ N, and stored at –80°C until analysis. Papaspyrou et al.: Properties of Pestarella tyrrhena burrows 183 Samples for determination of bacterial abundance Particulate iron. Samples for particulate iron analy- were taken in January and August 2002. Approximately sis were analysed according to the colorimetric method 300 mg sediment from a single burrow was transferred of Lovley & Phillips (1987). Briefly, 300 mg of sediment to a pre-weighed sterile Eppendorf tube containing 1 ml was immediately transferred after collection to
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